Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T13:28:23.325Z Has data issue: false hasContentIssue false
  • English
  • Français

Desiccation damage, accelerated ageing and respiration in desiccation tolerant and sensitive seeds

Published online by Cambridge University Press:  22 February 2007

Christina Walters ,
N.W. Pammenter ,
Patricia Berjak  and
Jennifer Crane
Christina Walters*
Affiliation:
USDA-ARS, National Seed Storage Laboratory, 1111 S. Mason St., Fort Collins, CO 80524, USA
N.W. Pammenter
Affiliation:
Plant Cell Biology Research Unit, Department of Biology, University of Natal, King George V Avenue, Durban, 4001, South Africa
Patricia Berjak
Affiliation:
Plant Cell Biology Research Unit, Department of Biology, University of Natal, King George V Avenue, Durban, 4001, South Africa
Jennifer Crane
Affiliation:
USDA-ARS, National Seed Storage Laboratory, 1111 S. Mason St., Fort Collins, CO 80524, USA
*
*Correspondence Tel.: 970-495-3202 Fax: 970-221-1427 Email: chrisv@lamar.colostate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Embryonic axes of tea (desiccation sensitive) and pea (desiccation tolerant) were dried at different rates or stored at different water contents to distinguish between damage associated with the immediate effects of water loss and the longer-term effects of a partially hydrated state. No loss of viability was observed if pea axes were dried sufficiently rapidly (from 1.8 to 0.1 g H2O g-1dry mass (g/g) within 5 d). However, viability was lost in tea axes dried below 0.5 g/g (approximately -15 MPa) even if axes were dried within 1 h. Death in tea axes dried to moisture contents less than 0.5 g/g probably resulted from the removal of water necessary for cellular structural integrity (i.e. desiccation damage sensu stricto). When axes of both species were dried at slower rates, viability losses were observed at water potentials between about -3 and -15 MPa. The timing for this type of damage was species dependent, occurring within 2 d for tea and after 5 d for pea, and may be explained by higher oxidative activity in tea compared to pea. Embryos of both species with water potentials below -3 MPa were lethally damaged if oxygen consumption exceeded 1000–5000 μmol O2 g-1dry mass. Recalcitrant seeds are different than orthodox seeds because the former do not survive drying below a critical water content, regardless of the drying rate. Rapid drying is required for accurate assessment of the critical water content. Slow drying leads to metabolic imbalance and artefactual assessment of the critical water content for desiccation damage. Both tea and pea seeds were susceptible to damage from metabolic imbalances, suggesting that the predominant stress from slow drying is ageing.

Keywords

accelerated ageingdesiccation damagedesiccation tolerancegerminationorthodox seedsoxidative damagerecalcitrant seedsrespirationseedwater contentwater potential
Type
Research Article
Information
Seed Science Research , Volume 11 , Issue 2 , June 2001 , pp. 135 - 148
Copyright
Copyright © Cambridge University Press 2001

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, C.A., Fjerstad, M.C. and Rinne, R.W. (1983) Characteristics of soybean seed maturation: Necessity for slow dehydration. Crop Science 23, 265–267.CrossRefGoogle Scholar
Berjak, P., Farrant, J.M. and Pammenter, N.W. (1989) The basis of recalcitrant seed behaviour: cell biology of the homoiohydrous seed condition. pp. 89–108 in Taylorson, R.B. (Ed.) Recent advances in the development and germination of seeds. New York, Plenum Press.CrossRefGoogle Scholar
Berjak, P., Vertucci, C.W. and Pammenter, N.W. (1993) Effects of developmental status and dehydration rate on characteristics of water and desiccation-sensitivity in recalcitrant seeds of Camellia sinensis. Seed Science Research 3, 155–166.CrossRefGoogle Scholar
Bradford, K.J. (1995) Water relations in seed germination. pp. 351–398 in Kigel, J.; Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker Inc.Google Scholar
Chandler, P.M. and Robertson, M. (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Annual Review of Plant Physiology and Molecular Biology 45, 113–141.CrossRefGoogle Scholar
Chaudhury, R., Radhamani, J. and Chandel, K.P.S. (1991) Preliminary observations on the cryopreservation of desiccated embryonic axes of tea (Camellia sinensis (L.) O. Kuntze) seeds for genetic conservation. Cryo-Letters 12, 31–36.Google Scholar
Clegg, J.S. (1986) The physical properties and metabolic status of Artemia cysts at low water content: the ‘Water Replacement Hypothesis’. pp. 169–187 in Leopold, A.C. (Ed.) Membranes, metabolism and dry organisms. Ithaca, NY, Cornell University Press.Google Scholar
Dahal, P., Kim, N-S. and Bradford, K.J. (1996) Respiration and germination rates of tomato seeds at suboptimal temperatures and reduced water potentials. Journal of Experimental Botany 47, 941–947.CrossRefGoogle Scholar
Delouche, J.C. and Baskin, C.C. (1973) Accelerated aging techniques for predicting the relative storability of seed lots. Seed Science and Technology 1, 427–452.Google Scholar
Dickie, J.B., May, K., Morris, S.V.A. and Titley, S.E. (1991) The effects of desiccation on seed survival in Acer platanoides L. and Acer pseudoplatanus L. Seed Science Research 1, 149–162.CrossRefGoogle Scholar
Farrant, J.M. and Walters, C. (1998) Ultrastructural and biophysical changes in developing embryos of Aesculus hippocastanum in relation to the acquisition of tolerance to drying. Physiologia Plantarum 104, 513–524.CrossRefGoogle Scholar
Farrant, J.M., Berjak, P. and Pammenter, N.W. (1985) The effect of drying rate on viability retention of recalcitrant propagules of Avicennia marina. South African Journal of Botany 51, 432–438.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1986) The increasing desiccation sensitivity of recalcitrant Avicennia marina seeds with storage time. Physiologia Plantarum 67, 291–298.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1989) Germination associated events and the desiccation sensitivity of recalcitrant seeds – a study on three unrelated species. Planta 178, 189–198.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W., Berjak, P. and Walters, C. (1997) Subcellular organisation and metabolic activity during the development of seeds that attain different levels of desiccation tolerance. Seed Science Research 7, 135–144.CrossRefGoogle Scholar
Finch-Savage, W.E. (1992) Embryo water status and survival in the recalcitrant species Quercus robur L.: Evidence for a critical moisture content. Journal of Experimental Botany 43, 663–669.CrossRefGoogle Scholar
Finch-Savage, W.E., Hendry, G.A.F. and Atherton, N.M. (1994) Free radical activity and loss of viability during drying of desiccation-sensitive tree seeds. Proceedings of the Royal Society of Edinburgh 102B, 257–260.Google Scholar
Hand, S.C. and Hardewig, I. (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annual Review of Physiology 58, 539–563.CrossRefGoogle ScholarPubMed
Hay, F.R. and Probert, R.J. (1995) Seed maturity and the effects of different drying conditions on desiccation tolerance and seed longevity in foxglove (Digitalis purpurea L.). Annals of Botany 76, 639–647.CrossRefGoogle Scholar
Hendry, G.A.F., Finch-Savage, W.E., Thorpe, P.C., Atherton, N.M., Buckland, S.M., Nilsson, K.A. and Seel, W.E. (1992) Free radical processes and loss of seed viability during desiccation in the recalcitrant species Quercus robur L. New Phytologist 122, 273–279.CrossRefGoogle ScholarPubMed
Hong, T.D. and Ellis, R.H. (1997) The effect of the initial rate of drying on the subsequent ability of immature seeds of Norway maple (Acer platanoides L.) to survive rapid desiccation. Seed Science Research 7, 41–45.CrossRefGoogle Scholar
Hu, J., Guo, C.G. and Shi, S.X. (1993) Partial drying and post thaw preconditioning improve the survival and germination of cryopreserved seeds of tea (Camellia sinensis). FAO/IBPGR Plant Genetic Resources Newsletter 93, 1–4.Google Scholar
Ibrahim, A.E., Roberts, E.H. and Murdoch, A.J. (1983) Viability of lettuce seeds II. Survival and oxygen uptake in osmotically controlled storage. Journal of Experimental Botany 34, 631–640.CrossRefGoogle Scholar
Kermode, A.R. (1995) Regulatory mechanisms in the transition from seed development to germination: Interactions between the embryo and the seed environment. pp. 273–332 in Kigel, J.; Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker Inc.Google Scholar
Kuranuki, Y. and Yoshida, S. (1996) Different responses of embryonic axes and cotyledons from tea seeds to desiccation and cryoexposure. Breeding Science 46, 149–154.Google Scholar
Leprince, O. and Hoekstra, F.A. (1998) The responses of cytochrome redox state and energy metabolism to dehydration support a role for cytoplasmic viscosity in desiccation tolerance. Plant Physiology 118, 1253–1264.CrossRefGoogle ScholarPubMed
Leprince, O., Deltour, R., Thorpe, P.C., Atherton, N.M. and Hendry, G.A.F. (1990) The role of free radicals and radical processing systems in loss of desiccation tolerance in germinating maize (Zea mays L.). New Phytologist 116, 573–580.CrossRefGoogle Scholar
Leprince, O., van der Werf, A., Deltour, R. and Lambers, H. (1992) Respiratory pathways in germinating maize radicles correlated with desiccation tolerance and soluble sugars. Physiologia Plantarum 85, 581–588.CrossRefGoogle Scholar
Leprince, O., Hendry, G.A.F. and McKersie, B.D. (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Science Research 3, 231–246.CrossRefGoogle Scholar
Leprince, O., Atherton, N.M., Deltour, R. and Hendry, G.A.F. (1994) The involvement of respiration in freeradical processes during loss of desiccation tolerance in germinating Zea mays L. An electron paramagnetic resonance study. Plant Physiology 104, 1333–1339.CrossRefGoogle Scholar
Leprince, O., Vertucci, C.W., Hendry, G.A.F. and Atherton, N.M. (1995) The expression of desiccation-induced damage in orthodox seeds is a function of oxygen and temperature. Physiologia Plantarum 94, 233–240.CrossRefGoogle Scholar
Leprince, O., Buitink, J. and Hoekstra, F.A. (1999) Axes and cotyledons of recalcitrant seeds of Castanea sativa Mill. exhibit contrasting responses of respiration to drying in relation to desiccation sensitivity. Journal of Experimental Botany 50, 1515–1524.CrossRefGoogle Scholar
Leprince, O., Harren, F.J.M., Buitink, J., Alberda, M. and Hoekstra, F.A. (2000) Metabolic dysfunction and unabated respiration precede the loss of membrane integrity during dehydration of germinating radicles. Plant Physiology 122, 597–608.CrossRefGoogle ScholarPubMed
Levitt, J. (1980) Responses of plants to environmental stresses. Volume II. Water, radiation, salt and other stress. New York, Academic Press.Google Scholar
McKersie, B.D., Senaratna, T., Walker, M.A., Kendall, E.J. and Hetherington, P.R. (1988) Deterioration of membranes during aging in plants: evidence for free radical mediation. pp. 441–464 in Noodén, L.D.; Leopold, A.C. (Eds) Senescence and aging in plants. New York, Academic Press.Google Scholar
Michel, B.E. and Kaufmann, M.R. (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiology 51, 914–916.CrossRefGoogle ScholarPubMed
Murashige, T. and Skoog, E. (1962) A revised medium for rapid growth and bioassays with tobacco tissues cultures. Physiologia Plantarum 15, 473–497.CrossRefGoogle Scholar
Normah, M.N., Chin, H.F. and Hor, Y.L. (1986) Desiccation and cryostorage of embryonic axes of Hevea brasiliensis Muell.-Afg. Pertanika 9, 299–303.Google Scholar
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccationtolerance mechanisms. Seed Science Research 9, 13–37.CrossRefGoogle Scholar
Pammenter, N.W., Vertucci, C.W. and Berjak, P. (1991) Homeohydrous (recalcitrant) seeds: dehydration, the state of water and viability characteristics in Landolphia kirkii. Plant Physiology 96, 1093–1098.CrossRefGoogle ScholarPubMed
Pammenter, N.W., Greggains, V., Kioko, J.I., Wesley-Smith, J., Berjak, P. and Finch-Savage, W.E. (1998) Effects of differential drying rates on viability retention of recalcitrant seeds of Ekebergia capensis. Seed Science Research 8, 463–471.CrossRefGoogle Scholar
Petruzzelli, L. (1986) Wheat viability at high moisture content under hermetic and aerobic storage conditions. Annals of Botany 58, 259–265.CrossRefGoogle Scholar
Powell, A.D., Dulson, J. and Bewley, J.D. (1984) Changes in germination and respiratory potential of embryos of dormant Grand Rapids lettuce seeds during long-term imbibed storage, and related changes in the endosperm. Planta 162, 40–45.CrossRefGoogle Scholar
Pritchard, H.W. (1991) Water potential and embryonic axis viability in recalcitrant seeds of Quercus rubra. Annals of Botany 67, 43–49.CrossRefGoogle Scholar
Pritchard, H.W. and Manger, K.R. (1998) A calorimetric perspective on desiccation stress during preservation procedures with recalcitrant seeds of Quercus robur L. CryoLetters 19 (suppl. 1), 23–30.Google Scholar
Pritchard, H.W. and Prendergast, F.G. (1986) Effects of desiccation and cryopreservation on the in vitro viability of embryos of the recalcitrant seed species Araucaria hunsteinii K. Shum. Journal of Experimental Botany 37, 1388–1397.CrossRefGoogle Scholar
Probert, R.J. and Longley, P.L. (1989) Recalcitrant seed storage physiology in three aquatic grasses (Zizania palustris, Spartina anglica and Porteresia coarctata). Annals of Botany 63, 53–63.CrossRefGoogle Scholar
Puntarulo, S., Galleano, M., Sanchez, R.A. and Boveris, A. (1991) Superoxide anion and hydrogen peroxide metabolism in soybean embryonic axes during germination. Biochimica et Biophysica Acta 1074, 277–283.CrossRefGoogle ScholarPubMed
Ried, J. and Walker-Simmons, M.K. (1993) Group 3 late embryogenesis abundant proteins in desiccation tolerant seedlings of wheat (Triticum aestivum L.). Plant Physiology 102, 125–131.CrossRefGoogle ScholarPubMed
Roberts, E.H. (1973) Predicting the storage life of seeds. Seed Science and Technology 1, 499–514.Google Scholar
Roberts, E.H. and Ellis, R.H. (1989) Water and seed survival. Annals of Botany 63, 39–52.CrossRefGoogle Scholar
Salmen-Espindola, L., Noin, M., Corbineau, F. and Côme, D. (1994) Cellular and metabolic damage induced by desiccation in recalcitrant Araucaria angustifolia embryos. Seed Science Research 4, 193–201.CrossRefGoogle Scholar
Senaratna, T. and McKersie, B.D. (1983) Dehydration injury in germinating soybean (Glycine max L. Merr.) seeds. Plant Physiology 72, 620–624.CrossRefGoogle ScholarPubMed
TeKrony, D.M. and Egli, D.B. (1997) Accumulation of seed vigour during development and maturation. pp. 368–384 in Ellis, R.H.; Black, M.; Murdoch, A.J.; Hong, T.D. (Eds) Basic and applied aspects of seed biology. Dordrecht, Kluwer Academic Publishers.Google Scholar
Tompsett, P.B. (1983) The influence of gaseous environment on the storage life of Araucaria hunsteinii seed. Annals of Botany 52, 229–237.CrossRefGoogle Scholar
Vertucci, C.W. (1990) Calorimetric studies of the state of water in seed tissues. Biophysical Journal 58,1463–1471.CrossRefGoogle ScholarPubMed
Vertucci, C.W. and Farrant, J.M. (1995) Acquisition and loss of desiccation tolerance. pp. 237–271 in Kigel, J.; Galili, G. (Eds) Seed development and germination. New York, Marcel Dekker Inc.Google Scholar
Vertucci, C.W. and Leopold, A.C. (1984) Bound water in soybean seed and its relation to respiration and imbibitional damage. Plant Physiology 75, 114–117.CrossRefGoogle ScholarPubMed
Villiers, T.A. (1975) Genetic maintenance of seeds in imbibed storage. pp. 297–315 in Frankel, O.H; Hawkes, J.G. (Eds) Crop genetic resources for today and tomorrow. Cambridge, Cambridge University Press.Google Scholar
Walters, C., Ried, J.L. and Walker-Simmons, M.K. (1997) Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties. Seed Science Research 7, 125–134.CrossRefGoogle Scholar
Walters, C., Pammenter, N.W., Berjak, P. and Farrant, J.M. (2001) Desiccation stress and damage. in Black, M.; Pritchard, H.W. (Eds) Desiccation and plant survival. Wallingford, CABI Publishing (in press).Google Scholar
Wolfe, J. and Bryant, G. (1999) Freezing, drying and/or vitrification of membrane-solute-water systems. Cryobiology 39, 103–129.CrossRefGoogle ScholarPubMed